Endosymbiotic bioenergetic synergy behind adaptation and speciation of rainforest warblers

Dahong Chen, Silu Wang

The molecular genetic cooperation among organelles facilitates adaptation during eukaryotic evolution, but the composition of such endosymbiotic synergy in the organismal adaptation and speciation remains unclear. The speciating wood warblers hybridizing in the Pacific Rainforest experiencing dramatic climate changes provide natural inter-organelle-recombination experiments to understand the molecular genomic processes associated with speciation and adaptation in the changing world. Integrating life history morphometrics, cell-type-specific multiomics, biochemical analyses and confocal imaging, we discovered the endosymbiotic bioenergetic synergy among nucleus, mitochondria, and ribosome at the molecular genomic frontier of divergent climate adaptation. We further identified signatures of adaptive inertia in populations underwent drastic climate change, which corresponds with endosymbiotic uncoupling and reduced energy capacity. Remarkably, endosymbiotic co-transcriptional synergy can be rescued by the introgression of warm-adapted endosymbiotic genetic variants across the species boundaries despite the risk of endosymbiotic bioenergetic incompatibility brought by ancestry discordance. This study inspires the Endosymbiotic Bioenergetic Synergy Model, which characterizes the molecular genomic cofunction, co-regulation, coevolution, and co-introgression among organelles underlying bioenergetic adaptation and speciation of eukaryotes. This endosymbiotic synergistic insight illuminates further investigation of bioenergetic adaptation of eukaryotic species over space and time.